Efficient generation of mucosal and systemic antigen-specific CD8 + T-cell responses following pulmonary DNA immunization

Journal of Virology

Volumn 84, Issue 11, 2010, Pages 5764-5774

  Bivas Benita, Maytal ^a   Bar, Liat ^a   Gillard, Geoffrey O ^a   Kaufman, David R ^a   Simmons, Nathaniel L ^a   Hovav, Avi Hai ^b   Letvin, Norman L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2; PLASMID DNA; POLYETHYLENEIMINE;

ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; BAGG ALBINO MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CYTOKINE PRODUCTION; DNA IMMUNIZATION; FEMALE; GENE EXPRESSION; GENE TARGETING; INTESTINE; LUNG CAVITY; MOUSE; MUCOSA CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION; VAGINA MUCOSA;

ANIMALS; ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DRUG ADMINISTRATION ROUTES; FEMALE; IMMUNIZATION; INTESTINAL MUCOSA; LUNG; MICE; MUCOUS MEMBRANE; PLASMIDS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; VAGINA;

MUS; VACCINIA VIRUS;

EID: 77951992275     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02202-09     Document Type: Article

References (41)

1. Bachmann, M. F., P. Wolint, K. Schwarz, P. Jager, and A. Oxenius. 2005. Functional properties and lineage relationship of CD8+ T-cell subsets identified by expression of IL-7 receptor alpha and CD62L. J. Immunol. 175:4686-4696.
2. Barnett, S. W., I. K. Srivastava, E. Kan, F. Zhou, A. Goodsell, A. D. Cristillo, M. G. Ferrai, D. E. Weiss, N. L. Letvin, D. Montefiori, R. Pal, and M. Vajdy. 2008. Protection of macaques against vaginal SHIV challenge by systemic or mucosal and systemic vaccinations with HIV-envelope. AIDS 22:339-348.
3. Belyakov, I. M., D. Isakov, Q. Zhu, A. Dzutsev, and J. A. Berzofsky. 2007. A novel functional CTL avidity/activity compartmentalization to the site of mucosal immunization contributes to protection of macaques against simian/human immunodeficiency viral depletion of mucosal CD4+ T cells. J. Immunol. 178:7211-7221.
4. Bivas-Benita, M., M. Y. Lin, S. M. Bal, K. E. van Meijgaarden, K. L. Franken, A. H. Friggen, H. E. Junginger, G. Borchard, M. R. Klein, and T. H. Ottenhoff. 2009. Pulmonary delivery of DNA encoding Mycobacterium tuberculosis latency antigen Rv1733c associated to PLGA-PEI nanoparticles enhances T-cell responses in a DNA prime/protein boost vaccination regimen in mice. Vaccine 27:4010-4017.
5. Bivas-Benita, M., R. Zwier, H. E. Junginger, and G. Borchard. 2005. Noninvasive pulmonary aerosol delivery in mice by the endotracheal route. Eur. J. Pharm. Biopharm. 61:214-218.
6. Bonnet, M. E., P. Erbacher, and A. L. Bolcato-Bellemin. 2008. Systemic delivery of DNA or siRNA mediated by linear polyethylenimine (L-PEI) does not induce an inflammatory response. Pharm. Res. 25:2972-2982.
7. Breuzard, G., M. Tertil, C. Goncalves, H. Cheradame, P. Geguan, C. Pichon, and P. Midoux. 2008. Nuclear delivery of NFkappaB-assisted DNA/polymer complexes: plasmid DNA quantitation by confocal laser scanning microscopy and evidence of nuclear polyplexes by FRET imaging. Nucleic Acids Res. 36:e71. (Pubitemid 351984839)
8. Brunner, S., E. Furtbauer, T. Sauer, M. Kursa, and E. Wagner. 2002. Overcoming the nuclear barrier: cell cycle independent nonviral gene transfer with linear polyethylenimine or electroporation. Mol. Ther. 5:80-86.
9. Chen, H. H., Y. P. Ho, X. Jiang, H. Q. Mao, T. H. Wang, and K. W. Leong. 2008. Quantitative comparison of intracellular unpacking kinetics of polyplexes by a model constructed from quantum dot-FRET. Mol. Ther. 16:324-332.
10. de Bree, G. J., H. Daniels, M. Schilfgaarde, H. M. Jansen, T. A. Out, R. A. van Lier, and R. E. Jonkers. 2007. Characterization of CD4+ memory T-cell responses directed against common respiratory pathogens in peripheral blood and lung. J. Infect. Dis. 195:1718-1725.
11. Deliyannis, G., K. Kedzierska, Y. F. Lau, W. Zeng, S. J. Turner, D. C. Jackson, and L. E. Brown. 2006. Intranasal lipopeptide primes lung-resident memory CD8+ T cells for long-term pulmonary protection against influenza. Eur. J. Immunol. 36:770-778.
12. Demeneix, B., and J. P. Behr. 2005. Polyethylenimine (PEI). Adv. Genet. 53:217-230.
13. Gallichan, W. S., and K. L. Rosenthal. 1996. Long-lived cytotoxic T lymphocyte memory in mucosal tissues after mucosal but not systemic immunization. J. Exp. Med. 184:1879-1890.
14. Gautam, A., C. L. Densmore, E. Golunski, B. Xu, and J. C. Waldrep. 2001. Transgene expression in mouse airway epithelium by aerosol gene therapy with PEI-DNA complexes. Mol. Ther. 3:551-556.
15. Gautam, A., C. L. Densmore, B. Xu, and J. C. Waldrep. 2000. Enhanced gene expression in mouse lung after PEI-DNA aerosol delivery. Mol. Ther. 2:63-70.
16. Hamann, D., P. A. Baars, M. H. Rep, B. Hooibrink, S. R. Kerkhof-Garde, M. R. Klein, and R. A. van Lier. 1997. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186:1407-1418.
17. Hendriks, J., L. A. Gravestein, K. Tesselaar, R. A. van Lier, T. N. Schumacher, and J. Borst. 2000. CD27 is required for generation and long-term maintenance of T-cell immunity. Nat. Immunol. 1:433-440.
18. Hendriks, J., Y. Xiao, and J. Borst. 2003. CD27 promotes survival of activated T cells and complements CD28 in generation and establishment of the effector T-cell pool. J. Exp. Med. 198:1369-1380.
19. Hikono, H., J. E. Kohlmeier, K. H. Ely, I. Scott, A. D. Roberts, M. A. Blackman, and D. L. Woodland. 2006. T-cell memory and recall responses to respiratory virus infections. Immunol. Rev. 211:119-132.
20. Hintzen, R. Q., R. de Jong, S. M. Lens, and R. A. van Lier. 1994. CD27: marker and mediator of T-cell activation? Immunol. Today 15:307-311.
21. Hogan, R. J., W. Zhong, E. J. Usherwood, T. Cookenham, A. D. Roberts, and D. L. Woodland. 2001. Protection from respiratory virus infections can be mediated by antigen-specific CD4(+) T cells that persist in the lungs. J. Exp. Med. 193:981-986.
22. Holmgren, J., and C. Czerkinsky. 2005. Mucosal immunity and vaccines. Nat. Med. 11:S45-53.
23. Hovav, A. H., M. W. Panas, C. E. Osuna, M. J. Cayabyab, P. Autissier, and N. L. Letvin. 2007. The impact of a boosting immunogen on the differentiation of secondary memory CD8+ T cells. J. Virol. 81:12793-12802.
24. Jakubzick, C., J. Helft, T. J. Kaplan, and G. J. Randolph. 2008. Optimization of methods to study pulmonary dendritic cell migration reveals distinct capacities of DC subsets to acquire soluble versus particulate antigen. J. Immunol. Methods 337:121-131.
25. Jeyanathan, M., J. Mu, K. Kugathasan, X. Zhang, D. Damjanovic, C. Small, M. Divangahi, B. J. Petrof, C. M. Hogaboam, and Z. Xing. 2008. Airway delivery of soluble mycobacterial antigens restores protective mucosal immunity by single intramuscular plasmid DNA tuberculosis vaccination: role of proinflammatory signals in the lung. J. Immunol. 181:5618-5626.
26. Kaufman, D. R., J. Liu, A. Carville, K. G. Mansfield, M. J. Havenga, J. Goudsmit, and D. H. Barouch. 2008. Trafficking of antigen-specific CD8+ T lymphocytes to mucosal surfaces following intramuscular vaccination. J. Immunol. 181:4188-4198.
27. Kichler, A., C. Leborgne, E. Coeytaux, and O. Danos. 2001. Polyethylenimine-mediated gene delivery: a mechanistic study. J. Gene Med. 3:135-144. (Pubitemid 33685440)
28. Klavinskis, L. S., C. Barnfield, L. Gao, and S. Parker. 1999. Intranasal immunization with plasmid DNA-lipid complexes elicits mucosal immunity in the female genital and rectal tracts. J. Immunol. 162:254-262.
29. Lagranderie, M., P. Ravisse, G. Marchal, M. Gheorghiu, V. Balasubramanian, E. H. Weigeshaus, and D. W. Smith. 1993. BCG-induced protection in guinea pigs vaccinated and challenged via the respiratory route. Tuberc. Lung Dis. 74:38-46.
30. Masopust, D., V. Vezys, E. J. Usherwood, L. S. Cauley, S. Olson, A. L. Marzo, R. L. Ward, D. L. Woodland, and L. Lefrancois. 2004. Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J. Immunol. 172:4875-4882. (Pubitemid 38456411)
31. Pollard, H., J. S. Remy, G. Loussouarn, S. Demolombe, J. P. Behr, and D. Escande. 1998. Polyethylenimine but not cationic lipids promotes transgene delivery to the nucleus in mammalian cells. J. Biol. Chem. 273:7507-7511.
32. Reina, R., C. Barbezange, H. Niesalla, X. de Andres, H. Arnarson, E. Biescas, M. Mazzei, C. Fraisier, T. N. McNeilly, C. Liu, M. Perez, M. L. Carrozza, P. Bandecchi, C. Solano, H. Crespo, I. Glaria, C. Huard, D. J. Shaw, I. de Blas, D. de Andres, F. Tolari, S. Rosati, M. Suzan-Monti, V. Andresdottir, S. Torsteinsdottir, G. Petursson, L. Lujan, M. Pepin, B. Amorena, B. Blacklaws, and G. D. Harkiss. 2008. Mucosal immunization against ovine lentivirus using PEI-DNA complexes and modified vaccinia Ankara encoding the gag and/or env genes. Vaccine 26:4494-4505.
33. Santosuosso, M., S. McCormick, X. Zhang, A. Zganiacz, and Z. Xing. 2006. Intranasal boosting with an adenovirus-vectored vaccine markedly enhances protection by parenteral Mycobacterium bovis BCG immunization against pulmonary tuberculosis. Infect. Immun. 74:4634-4643.
34. Sonawane, N. D., F. C. Szoka, Jr., and A. S. Verkman. 2003. Chloride accumulation and swelling in endosomes enhances DNA transfer by polyamine-DNA polyplexes. J. Biol. Chem. 278:44826-44831.
35. Staats, H. F., C. P. Bradney, W. M. Gwinn, S. S. Jackson, G. D. Sempowski, H. X. Liao, N. L. Letvin, and B. F. Haynes. 2001. Cytokine requirements for induction of systemic and mucosal CTL after nasal immunization. J. Immunol. 167:5386-5394.
36. Takahashi, H., Y. Nakagawa, C. D. Pendleton, R. A. Houghten, K. Yokomuro, R. N. Germain, and J. A. Berzofsky. 1992. Induction of broadly cross-reactive cytotoxic T cells recognizing an HIV-1 envelope determinant. Science 255:333-336.
37. Wayne Conlan, J., H. Shen, R. Kuolee, X. Zhao, and W. Chen. 2005. Aerosol-, but not intradermal-immunization with the live vaccine strain of Francisella tularensis protects mice against subsequent aerosol challenge with a highly virulent type A strain of the pathogen by an alphabeta T cell- and interferon gamma-dependent mechanism. Vaccine 23:2477-2485.
38. Wee, J. L., J. P. Scheerlinck, K. J. Snibson, S. Edwards, M. Pearse, C. Quinn, and P. Sutton. 2008. Pulmonary delivery of ISCOMATRIX influenza vaccine induces both systemic and mucosal immunity with antigen dose sparing. Mucosal Immunol. 1:489-496.
39. Wikstrom, M. E., and P. A. Stumbles. 2007. Mouse respiratory tract dendritic cell subsets and the immunological fate of inhaled antigens. Immunol. Cell Biol. 85:182-188.
40. Woodland, D. L., and J. E. Kohlmeier. 2009. Migration, maintenance and recall of memory T cells in peripheral tissues. Nat. Rev. Immunol. 9:153-161.
41. Zammit, D. J., D. L. Turner, K. D. Klonowski, L. Lefrancois, and L. S. Cauley. 2006. Residual antigen presentation after influenza virus infection affects CD8 T-cell activation and migration. Immunity 24:439-449.